Annual Review of Phytopathology - Volume 58, 2020

Gall-inducing insects and nematodes engage in sophisticated interactions with their host plants. These parasites can induce major morphological and physiological changes in host roots, leaves, and other tissues. Sedentary endoparasitic nematodes, root-knot and cyst nematodes in particular, as well as gall-inducing and leaf-mining insects, manipulate plant development to form unique organs that provide them with food from feeding cells. Sometimes, infected tissues may undergo a developmental switch resulting in the formation of aberrant and spectacular structures (clubs or galls). We describe here the complex interactions between these plant-reprogramming sedentary endoparasites and their infected hosts, focusing on similarities between strategies of plant manipulation. We highlight progress in our understanding of the host plant response to infection and focus on the nematode and insect molecules secreted in planta. We suggest thatlooking at similarities may identify convergent and conserved strategies and shed light on the promise they hold for the development of new management strategies in agriculture and forestry.

Land plants host a vast and diverse virome that is dominated by RNA viruses, with major additional contributions from reverse-transcribing and single-stranded (ss) DNA viruses. Here, we introduce the recently adopted comprehensive taxonomy of viruses based on phylogenomic analyses, as applied to the plant virome. We further trace the evolutionary ancestry of distinct plant virus lineages to primordial genetic mobile elements. We discuss the growing evidence of the pivotal role of horizontal virus transfer from invertebrates to plants during the terrestrialization of these organisms, which was enabled by the evolution of close ecological associations between these diverse organisms. It is our hope that the emerging big picture of the formation and global architecture of the plant virome will be of broad interest to plant biologists and virologists alike and will stimulate ever deeper inquiry into the fascinating field of virus–plant coevolution.

Plant pathogens are a critical component of the microbiome that exist as populations undergoing ecological and evolutionary processes within their host. Many aspects of virulence rely on social interactions mediated through multiple forms of public goods, including quorum-sensing signals, exoenzymes, and effectors. Virulence and disease progression involve life-history decisions that have social implications with large effects on both host and microbe fitness, such as the timing of key transitions. Considering the molecular basis of sequential stages of plant–pathogen interactions highlights many opportunities for pathogens to cheat, and there is evidence for ample variation in virulence. Case studies reveal systems where cheating has been demonstrated and others where it is likely occurring. Harnessing the social interactions of pathogens, along with leveraging novel sensing and -omics technologies to understand microbial fitness in the field, will enable us to better manage plant microbiomes in the interest of plant health.

Increasing evidence indicates that tolerance is a host defense strategy against pathogens as widespread and successful as resistance. Since the concept of tolerance was proposed more than a century ago, it has been in continuous evolution. In parallel, our understanding of its mechanistic bases and its consequences for host and pathogen interactions, ecology, and evolution has grown. This review aims at summarizing the conceptual changes in the meaning of tolerance inside and outside the field of phytopathology, emphasizing difficulties in demonstrating and quantifying this trait. We also discuss evidence of tolerance and current knowledge on its genetic regulation, mechanisms, and role in host–pathogen coevolution, highlighting common patterns across hosts and pathogens. We hope that this comprehensive review attracts more plant pathologists to the study of this key plant defense response.

Non-native invasive plants can establish in natural areas, where they can be ecologically damaging and costly to manage. Like cultivated plants, invasive plants can experience a relatively disease-free period upon introduction and accumulate pathogens over time. Diseases of invasive plant populations are infrequently studied compared to diseases of agriculture, forestry, and even native plant populations. We evaluated similarities and differences in the processes that are likely to affect pathogen accumulation and disease in invasive plants compared to cultivated plants, which are the dominant focus of the field of plant pathology. Invasive plants experience more genetic, biotic, and abiotic variation across space and over time than cultivated plants, which is expected to stabilize the ecological and evolutionary dynamics of interactions with pathogens and possibly weaken the efficacy of infectious disease in their control. Although disease is expected to be context dependent, the widespread distribution of invasive plants makes them important pathogen reservoirs. Research on invasive plant diseases can both protect crops and help manage invasive plant populations.

Epigenetic mechanisms play fundamental roles in regulating numerous biological processes in various developmental and environmental contexts. Three highly interconnected epigenetic control mechanisms, including small noncoding RNAs, DNA methylation, and histone modifications, contribute to the establishment of plant epigenetic profiles. During the past decade, a growing body of experimental work has revealed the intricate, diverse, and dynamic roles that epigenetic modifications play in plant–nematode interactions. In this review, I summarize recent progress regarding the functions of small RNAs in mediating plant responses to infection by cyst and root-knot nematodes, with a focus on the functions of microRNAs. I also recapitulate recent advances in genome-wide DNA methylation analysis and discuss how cyst nematodes induce extensive and dynamic changes in the plant methylome that impact the transcriptional activity of genes and transposable elements. Finally, the potential role of nematode effector proteins in triggering such epigenome changes is discussed.

Focusing on the discovery and characterization of the Arabidopsis disease resistance protein RPS5 and its guardee PBS1, this review discusses work done in the Innes laboratory from the initial identification of the RPS5 gene in 1995 to the recent deployment of the PBS1 decoy system in crops. This is done through discussion of the structure, function, and signaling environment of RPS5 and PBS1, highlighting collaborations and influential ideas along the way. RPS5, a nucleotide-binding leucine-rich repeat (NLR) protein, is activated by the proteolytic cleavage of PBS1. We have shown that the cleavage site within PBS1 can be altered to contain cleavage sites for other proteases, enabling RPS5 activation by these proteases, thereby conferring resistance to different pathogens. This decoy approach has since been translated into crop species using endogenous PBS1 orthologs and holds strong potential for GMO-free development of new genetic resistance against important crop pathogens.

Public–private partnerships (PPPs) can be an effective and advantageous way to accomplish extension and outreach objectives in plant pathology. The greatest opportunities for extension-focused PPPs may be in response to large-scale or emerging disease management concerns or in addressing complex issues that impact agriculture, such as climate change, digital technology, and public perception of science. The most fertile ground for forming PPPs is where the needs and strengths of the public and private sectors are complementary. Developing PPPs depends as much on professional relationships as on technical skills or contracts. Defining and making room for the success of all partners, identifying and addressing barriers to success, and earning and maintaining trust are components that contribute to the effectiveness of PPPs. Case studies in plant pathology demonstrate the positive impact PPPs can have on partners and stakeholders and provide guidance on the formation of PPPs in the future.

During the Cold War, coffee became a strategically important crop in the global contest between the United States and the Soviet Union. The economies of many US allies in Latin America depended upon coffee. In the Cold War context, then, the coffee leaf rust (Hemileia vastatrix) became a geopolitical problem. Coffee experts in Latin America, which produced most of the world's coffee, began to prepare for an outbreak. In the 1950s, they built a global network of coffee experts. This network was sustained by US-led Cold War programs that promoted technical collaboration across the Global South, such as Harry Truman's Point Four programs. We explore the network's growth and evolution through one of its central figures, the American plant pathologist Frederick L. Wellman. This network has survived the end of the Cold War and evolved to reflect the new geopolitical context.

Plant pathogens have played an important role in weed biological control since the 1970s. So far, 36 fungal pathogens have been authorized for introduction across 18 countries for the classical biological control of weeds. Their safety record has been excellent, but questions continue to be asked about the risk that they could transfer to other plants. Quantitative data documenting their impact on the weed populations are still limited. Of the 15 bioherbicides based on living microorganisms that have ever been registered, only two were commercially available at the time of this review. The development and commercialization of bioherbicides in affluent countries are still plagued by technological hurdles and limited market potential. Not-for-profit small-scale production and distribution systems for bioherbicides in low-income countries may have potential as an inexpensive approach to controlling pervasive weeds. The types of research underpinning biological control approaches and challenges encountered are highlighted using specific examples.

Detection, identification, and quantification of plant diseases by sensor techniques are expected to enable a more precise disease control, as sensors are sensitive, objective, and highly available for disease assessment. Recent progress in sensor technology and data processing is very promising; nevertheless, technical constraints and issues inherent to variability in host–pathogen interactions currently limit the use of sensors in various fields of application. The information from spectral [e.g., RGB (red, green, blue)], multispectral, and hyperspectral sensors that measure reflectance, fluorescence, and emission of radiation or from electronic noses that detect volatile organic compounds released from plants or pathogens, as well as the potential of sensors to characterize the health status of crops, is evaluated based on the recent literature. Phytopathological aspects of remote sensing of plant diseases across different scales and for various purposes are discussed, including spatial disease patterns, epidemic spread of pathogens, crop characteristics, and links to disease control. Future challenges in sensor use are identified.

The EDS1 family of structurally unique lipase-like proteins EDS1, SAG101, and PAD4 evolved in seed plants, on top of existing phytohormone and nucleotide-binding–leucine-rich-repeat (NLR) networks, to regulate immunity pathways against host-adapted biotrophic pathogens. Exclusive heterodimers between EDS1 and SAG101 or PAD4 create essential surfaces for resistance signaling. Phylogenomic information, together with functional studies in Arabidopsis and tobacco, identify a coevolved module between the EDS1–SAG101 heterodimer and coiled-coil (CC) HET-S and LOP-B (CCHELO) domain helper NLRs that is recruited by intracellular Toll-interleukin1-receptor (TIR) domain NLR receptors to confer host cell death and pathogen immunity. EDS1–PAD4 heterodimers have a different and broader activity in basal immunity that transcriptionally reinforces local and systemic defenses triggered by various NLRs. Here, we consider EDS1 family protein functions across seed plant lineages in the context of networking with receptor and helper NLRs and downstream resistance machineries. The different modes of action and pathway connectivities of EDS1 family members go some way to explaining their central role in biotic stress resilience.

The loss of methyl bromide as a soil fumigant and minimal advances in the development and registration of new chemical fumigants has resulted in a resurgence of interest in the application of organic amendments (OAs) for soilborne plant pathogen and plant-parasitic nematode management. Significant progress has been made in the characterization of OAs, application of strategies for their use, and elucidation of mechanisms by which they suppress soilborne pests. Nonetheless, their utility is limited by the variability of disease control, expense, and the logistics of introducing them into crop production systems. Recent advances in molecular techniques have led to significant progress in the elucidation of the role of bacteria and fungi and their metabolic products on disease suppression with the addition of OAs. Biosolarization and anaerobic soil disinfestation, developed to manipulate systems and favor beneficial microorganisms to maximize their impact on plant pathogens, are built on a strong historical research foundation in OAs and the physical, chemical, and biological characteristics of disease-suppressive soils. This review focuses on recent applications of OAs and their potential for the management of soilborne plant pathogens and plant-parasitic nematodes, with emphasis primarily on annual fruit and vegetable production systems.

Plant pathology must contribute to improving food security in a safe operating space, which is shrinking as a result of declining natural resources, climate change, and the growing world population. This review analyzes the position of plant pathology in a nexus of relationships, which is mapped and where the coupled dynamics of crop growth, disease, and yield losses are modeled. We derive a hierarchy of pathogens, whereby pathogens reducing radiation interception (RI), radiation use efficiency (RUE), and harvest index increasingly impact crop yields in the approximate proportions: 1:4.5:4,700. Since the dawn of agriculture, plant breeding has targeted the harvest index as a main objective for domesticated plants. Surprisingly, the literature suggests that pathogens that reduce yields by directly damaging harvestable plant tissues have received much less attention than those that reduce RI or RUE. Ecological disease management needs to target diverse production situations and therefore must consider variation in attainable yields; this can be achieved through the reengineering of agrosystems to incorporate built-in dynamic diversity of genes, plants, and crop stands.

Global change is pressing forest pathologists to solve increasingly complex problems. We argue that understanding interactive effects between forest pathogens and global warming, globalization, and land-use changes may benefit from a functional ecology mindset. Traits can be more informative about ecological functions than species inventories and may deliver a more mechanistic description of forest disease. Myriad microbes with pathogenic potential interact with forest ecosystems at different organizational levels. Elucidation of functional traits may enable the microbial complexity to be reduced into manageable categories with predictive power. In this review, we propose guidelines that allow the research community to develop a functional forest pathology approach. We suggest new angles by which functional questions can be used to resolve burning issues on tree disease. Building up functional databases for pathogenicity is key to implementing these approaches.

False smut of rice, caused by Ustilaginoidea virens, has become one of the most important diseases in rice-growing regions worldwide. The disease causes a significant yield loss and imposes health threats to humans and animals by producing mycotoxins. In this review, we update our understanding of the pathogen, including the disease cycle and infection strategies, the decoding of the U. virens genome, comparative/functional genomics, and effector biology. Whereas the decoding of the U. virens genome unveils specific adaptations of the pathogen in successfully occupying rice flowers, progresses in comparative/functional genomics and effector biology have begun to uncover the molecular mechanisms underlying U. virens virulence and pathogenicity. We highlight the identification and characterization of the produced mycotoxins and their biosynthetic pathways in U. virens.The management strategies for this disease are also discussed. The flower-specific infection strategy makes the pathogen a unique tool to unveil novel mechanisms for the interactions between nonobligate biotrophic pathogens and their hosts.

The significance of water scarcity to crop production and food security has been globally recognized as a pivotal sustainability challenge in the UN Sustainable Development Goals (86). The critical link between water scarcity and sustainability is adaptation. Various changes in water use practices have been employed to alleviate production constraints. However, the potential for these changes to influence crop diseases has received relatively little attention, despite the circumglobal importance of diseases to agricultural sustainability. This article reviews what is known about the realized effects of scarcity-driven alterations in water use practices on diseases in the field in order to raise awareness of the potential for both increased disease risk and possible beneficial effects on crop disease management. This is followed by consideration of the primary mechanistic drivers underlying disease outcomes under various water use adaptation scenarios, concluding with a vision for disease–water co-management options and future research needs.